Journal of Experimental Botany

This Article Abstract FREE Full Text (PDF) E-letters: Submit a response Alert me when this article is cited Alert me when E-letters are posted Alert me if a correction is posted Services Email this article to a friend Similar articles in this journal Similar articles in ISI Web of Science Similar articles in PubMed Alert me to new issues of the journal Add to My Personal Archive Download to citation manager Search for citing articles in: ISI Web of Science (50) Request Permissions Disclaimer Google Scholar Articles by Cuin, T. A. Articles by Leigh, R. A. Search for Related Content PubMed PubMed Citation Articles by Cuin, T. A. Articles by Leigh, R. A. Agricola Articles by Cuin, T. A. Articles by Leigh, R. A. Social Bookmarking          What's this?

Journal of Experimental Botany, Vol. 54, No. 383, pp. 657-661, February 1, 2003
© 2003 Oxford University Press

Potassium activities in cell compartments of salt-grown barley leaves

Received 6 June 2002; Accepted 3 October 2002

Tracey Ann Cuin¹, Anthony J. Miller², Sophie A. Laurie³ and Roger A. Leigh^4,1

¹ Department of Plant Sciences, University of Cambridge, Downing Street, Cambridge CB2 3EA, UK
² Agriculture and Environment Division, Rothamsted Research, Harpenden, Hertfordshire AL5 2JQ, UK
³ Long Ashton Research Station, Department of Agricultural Sciences, University of Bristol, Long Ashton, Bristol BS18 9AF, UK

⁴ To whom correspondence should be addressed. Fax: +44 (0)1223 333953. E-mail: RL225{at}cam.ac.uk

	Abstract

Top Abstract Introduction Materials and methods Results Discussion References

 
Triple-barrelled microelectrodes measuring K⁺ activity (a_K), pH and membrane potential were used to make quantitative measurements of vacuolar and cytosolic a_K in epidermal and mesophyll cells of barley plants grown in nutrient solution with 0 or 200 mM added NaCl. Measurements of a_K were assigned to the cytosol or vacuole based on the pH measured. In epidermal cells, the salt treatment decreased a_K in the vacuole from 224 to 47 mM and in the cytosol from 68 to 15 mM. In contrast, the equivalent changes in the mesophyll were from 235 to 150 mM (vacuole) and 79 to 64 mM (cytosol). Thus mechanisms exist to ameliorate the effects of salt on a_K in compartments of mesophyll cells, presumably to minimize any deleterious consequences for photosynthesis. Thermodynamic calculations showed that K⁺ is actively transported into the vacuole of both epidermal and mesophyll cells of salinized and non- salinized plants. Comparison of the values of a_K in K⁺-replete, non-salinized leaf cells with those previously measured in root cells of plants grown under comparable conditions indicates that cytosolic a_K is similar in cells of both organs, but vacuolar a_K in leaf cells is approximately twice that in roots. This suggests differences in the regulation of vacuolar a_K, but not cytosolic a_K, in leaf and root cells.

Key words: Barley, cytosol, potassium, salinity, vacuole.

	Introduction

Top Abstract Introduction Materials and methods Results Discussion References

 
Soil salinity is estimated to affect between 340 and 950 million hectares of land worldwide and is a serious limitation to crop productivity because the majority of crop plants are not particularly salt tolerant (Flowers and Yeo, 1995). Therefore, much effort is being directed towards identifying the physiological and biochemical processes that are affected by NaCl with the aim of modifying these to increase salt tolerance (Apse and Blumwald, 2002). Compartmentation of Na⁺ and Cl^– in the vacuole is considered to be important in ameliorating the effects of salt on plants, and increasing Na⁺ transport into the vacuole has been shown to increase salt tolerance (Apse et al., 1999). In addition, the maintenance of a high cytosolic K⁺:Na⁺ ratio is also considered important (Maathuis and Amtmann, 1999). Thus, the capacity of plants to counteract salinity stress may strongly depend on their ability to compartment ions in the vacuole and to minimize ionic changes in the cytosol.

Although many studies have confirmed the sequestration of Na⁺ and Cl^– in the vacuole (Storey et al., 1983; Fricke et al., 1996), the behaviour of ions in the cytosol has been more difficult to determine because the small volume of this compartment makes quantitative measurements technically difficult. Those approaches that have been used, such as X-ray microanalysis (Storey et al., 1983; Flowers and Hajibagheri, 2001) and compartmental tracer efflux analysis (Yeo, 1981), generally support the hypothesis that maintenance of the cytosolic K⁺:Na⁺ ratio is important in salt tolerance. However, none of these techniques is fully quantitative and so accurate estimates of cytosolic ion concentrations in salinized plant cells are still lacking. In particular, measurements are needed in leaf cells because adverse effects of salinity in these are likely to have significant consequences for plant productivity. The lack of such measurements represents a significant impediment to testing hypotheses about responses of plants to salt and hence to identifying targets for manipulation. Another confounding aspect is that different cell types in leaves can be quite distinct in the ionic composition of their vacuoles (Leigh and Tomos, 1993; Karley et al., 2000), raising the possibility that cytosolic ion concentrations may also vary between cells, or may respond differently to salinity in different cell types. Differential responses of cytosolic K⁺ in epidermal and cortical cells of K⁺-deficient barley roots show that this is a real possibility (Walker et al., 1996).

Triple-barrelled microelectrodes measuring K⁺ activity (a_K), pH, and membrane potential (E_m) (Walker et al., 1995, 1996) can be used to make quantitative intracellular measurements of a_K in the vacuole and cytosol of cells in situ. The inclusion of the pH-sensing barrel allows assignment of a_K values to either the vacuole or the cytosol (Walker et al., 1995). In the study described here, such electrodes were used to measure quantitatively a_K in the vacuole and cytosol of leaf cells of barley plants grown in nutrient solutions with or without added NaCl. The results show that there is regulation of cytosolic a_K in response to salinity, but this is restricted to mesophyll cells; cytosolic a_K declines to very low levels in epidermal cells, although these remain viable. Comparison of the results with published data (Walker et al., 1996) indicates important similarities and differences in the regulation of cytosolic and vacuolar a_K in K⁺-replete leaf and root cells.

	Materials and methods

Top Abstract Introduction Materials and methods Results Discussion References

 
Plant material and whole-tissue measurements
Barley (Hordeum vulgare L. cv. Gerbel) seeds were germinated and grown in a modified Hoagland’s nutrient solution containing 5 mM K⁺ (Walker et al., 1996). Plants were grown at a constant temperature of 20 °C with a photoperiod of 16 h, a photon flux density of approximately 300 µmol m^–2 s^–1 at plant height, and a relative humidity of 75%. Plants were grown in unamended nutrient solution for the first 7 d after germination and then the NaCl concentration in the nutrient solution of some of the plants was increased by 50 mM d^–1 to a final concentration of 200 mM. When treated in this way, the cultivar used, Gerbel, is relatively salt resistant (Flowers and Hajibagheri, 2001). All measurements were made on the third leaf from 21-d-old plants. This leaf had emerged and expanded after the salt treatment was imposed, and its responses to salt are similar to those of other leaves in barley (Greenway, 1962). The fresh weight and dry weight of the whole shoot and the third leaf were recorded for both control and salt-treated plants. Tissue was dried at 80 °C for 48 h. Measurements of tissue K⁺ and Na⁺ concentrations were made by atomic absorption spectrophotometry on sap extracts prepared according to Fricke et al. (1994) from 1 cm leaf sections taken from the region where measurements were made with microelectrodes. Tissue ion concentrations are expressed as mM in tissue water.

Electrophysiology
Triple-barrelled microelectrodes measuring a_K, pH and E_m were made and calibrated as described previously (Walker et al., 1995) except that the K⁺ sensor contained dibutyl sebacate as the plasticizer (Cuin et al., 1999). Potassium concentrations in calibration solutions were converted to a_K using activity coefficients of between 0.75 and 0.78 (Robinson and Stokes, 1959; Walker et al., 1995). Electrodes were inserted into cells half-way along the length of the third leaf of intact plants. Leaves were mounted on a Perspex holder with their lower edge touching a reservoir of dilute nutrient solution that also contained the reference bath electrode (Miller et al., 2001). This arrangement ensured that an electrical circuit was completed when the triple-barrelled microelectrode was inserted into the leaf. Leaves were placed on the holder at least 30 min before the measurements were made, and stomates remained open throughout the experiment. Impalements were made in cells of the ‘trough’ region of the upper epidermis (Fricke et al., 1995; Fricke, 1997) and on the first layer of mesophyll cells immediately beneath these. Mesophyll cells were accessed by pushing the electrode through an epidermal cell. Successful penetration was monitored by following the E_m, which became more negative when the electrode was within a cell. Values of a_K are expressed as mean and 95% confidence limits (Fry et al., 1990).

	Results

Top Abstract Introduction Materials and methods Results Discussion References

 
Treatment of the barley plants with NaCl adversely affected growth and significantly changed leaf ion concentrations. Compared with control (non-salinized) plants, the fresh weights of the whole shoot and third leaf decreased by 47% and 35%, respectively, in plants grown in 200 mM NaCl (Fig. 1A). This change was accompanied by a decrease in leaf K⁺ concentration and an increase in leaf Na⁺ concentration (Fig. 1B). These results are comparable with those reported by Flowers and Hajibagheri (2001) for the same barley variety grown under similar conditions.

View larger version (29K): [in this window] [in a new window]   Fig. 1. Fresh weights of the whole shoot and third leaf (A) and ion concentrations in the third leaf (B) of 21-d-old barley plants grown in nutrient solution containing 0 mM or 200 mM added NaCl. Results are mean ±SD (n=9).

 
Measurements of a_K were assigned to the vacuole or the cytosol on the basis of the accompanying pH measurements. In both epidermal and mesophyll cells, impalements yielded two populations of pH measurements with mean values of 7.1 and 5.1 (Table 1), which were taken to indicate insertions in the cytosol and vacuole, respectively (Walker et al., 1995, 1996). Compartmental pH values were not statistically different between epidermal and mesophyll cells, and were also unaffected by salinity. The mean values of E_m ranged from –83 to –91 mV in cells of non-salinized plants, but were 16 to 28 mV less negative in salinized plants, with the greatest effect on epidermal cell E_m (Table 1). There were no statistically-significant differences between E_m for impalements into the cytosol and the vacuole, suggesting that the E_m across the tonoplast was close to zero. This contrasts with Arabidopsis where Miller et al. (2001) measured a trans-tonoplast E_m of about –30 mV (cytosol with respect to the vacuole; Bertl et al., 1992).

View this table: [in this window] [in a new window]   Table 1. Vacuolar and cytosolic pH and membrane potentials (Em) in ‘trough’ cells of the upper epidermis and in mesophyll cells of the third leaf of 21-d-old barley plants grown in nutrient solution containing 0 or 200 mM added NaCl Values of Em were all measured with respect to the bath solution in which the lower edge of the leaf was immersed (see Materials and methods). Results are given as mean ±SD. The number of separate measurements is given in brackets.

 
In non-salinized plants, mean vacuolar a_K was 224 and 235 mM in epidermal and mesophyll cells, respectively, while the corresponding values in the cytosol were 68 and 79 mM (Table 2). Following growth in 200 mM NaCl, the mean vacuolar a_K in epidermal cells declined to 47 mM and a_K in the cytosol of these cells to 15 mM. In contrast, vacuolar a_K in mesophyll cells decreased only to 150 mM, while, in the cytosol, a_K declined to 64 mM.

View this table: [in this window] [in a new window]   Table 2. Compartmental aK in ‘trough’ cells of the upper epidermis and in mesophyll cells of the third leaf of 21-d-old barley plants grown in nutrient solution containing 0 or 200 mM added NaCl Results are given as mean and 95% confidence limits (Fry et al., 1990). The number of separate measurements is indicated in square brackets.

 

	Discussion

Top Abstract Introduction Materials and methods Results Discussion References

 
As far as is known, this paper reports the first quantitative measurements of cytosolic a_K in leaf cell compartments of plants subjected to salt stress. Overall, the results indicate that both vacuolar and cytosolic a_K in the mesophyll are maintained at the expense of the supply to the epidermis. The results are consistent with the observations by Fricke et al. (1996) who found, using single-cell sampling, that decreases in K⁺ concentrations and increases in Na⁺ concentrations were less in vacuoles of mesophyll cells than in those of epidermal cells when plants were grown at NaCl concentrations of 100 mM or more. This indicates that mechanisms exist to ameliorate ionic changes in leaf mesophyll cells, but not in epidermal cells. This may be a device to protect and maintain the photosynthetic activity of the mesophyll cells. However, since the fresh weight of the third leaf declined by 35% in the salt-treated plants, other changes must have affected growth detrimentally. For instance, it is possible that the decreases in a_K in epidermal cell compartments may ultimately be affecting some fundamental growth process. Testing the importance of changes in subcellular ion activities in response to salinity will require investigation to relate the ion activities to the rates of key physiological processes, as done for cytosolic a_K and protein synthesis in K⁺-deficient barley roots (Walker et al., 1998).

The differential behaviour of mesophyll and epidermal cells is similar to that seen in K⁺-deficient barley roots where cytosolic a_K declined to a much greater extent in epidermal cells than in cortical cells (Walker et al., 1996). These collective observations indicate that ion supplies to key cell types in both leaves and roots are protected in order to maintain their function in response to deficiencies or excesses of ions. How this is achieved in leaves is unclear, but the observation is consistent with work showing that epidermal and mesophyll cells have quite distinct ionic compositions (Leigh and Tomos, 1993; Karley et al., 2000). It seems clear that supply and/or retention of ions in different cell types is important in leaf function and in responses to ionic stresses.

Leigh and Wyn Jones (1984) proposed that cytosolic K⁺ concentrations are buffered by the mobilization of vacuolar K⁺. Measurements of cytosolic and vacuolar a_K in barley roots grown under a range of external K⁺ concentrations supported this contention, with cytosolic a_K declining only when the vacuolar a_K fell below about 25 mM (Walker et al., 1996). This does not seem to occur in leaf epidermal cells of salt-grown barley where cytosolic a_K declined to 15 mM despite the vacuole still containing about 50 mM K⁺ (Table 2). Why the vacuolar pool is not fully mobilized to maintain cytosolic a_K is unclear. It is unlikely to be due to the existence of a minimum K⁺ concentration below which the vacuolar pool cannot decline (as proposed by Leigh and Wyn Jones, 1984) because very low K⁺ concentrations can be measured in sap extracted from epidermal vacuoles of leaves of barley plants grown in 150 mM NaCl (Fricke et al., 1996). Therefore, it seems more likely that the maintenance of a high cytosolic a_K is not important in these cells, and so it declines, despite the availability of vacuolar K⁺. Fricke et al. (1996) observed large differences in K⁺ concentrations in vacuolar sap extracts from different epidermal cells of salt-grown leaves, so it is important that other cells are investigated in order to determine whether the behaviour of vacuolar and cytosolic a_K observed in upper epidermal ‘trough’ cells is typical of all epidermal cells.

At 15 mM, the cytosolic a_K in the ‘trough’ epidermal cells from the salt-grown plants was at levels considered inadequate to support key K⁺-dependent functions such as protein synthesis (Lubin and Ennis, 1964; Leigh and Wyn Jones, 1984; Walker et al., 1998). It therefore seems unlikely that these cells are particularly metabolically active. Nonetheless, they appear to retain their viability, as evident by (1) a relatively negative E_m, indicating that their plasma membrane is intact and ion transporters functioning; (2) a near-neutral cytosolic pH, which, at the measured values of E_m and a typical leaf apoplastic pH of about 5.5 (Mühling and Läuchli, 2000), could only be maintained by active H⁺ extrusion; and (3) a turgor of approximately 0.9 MPa with correspondingly high sap osmotic pressure and ion concentrations (Fricke, 1997; Fricke et al., 1996). Thus, cytosolic a_K values below those normally considered optimal for protein synthesis do not necessarily lead to a loss of viability of epidermal cells.

The compartment-specific values of E_m, pH and a_K obtained with the triple-barrelled microelectrodes provide sufficient information to make thermodynamic calculations of the direction of active K⁺ transport at the tonoplast, and the feasibility of different active transport mechanisms (see Walker et al., 1996, for equations). These calculations (results not presented) show that for both epidermal and mesophyll cells, under both sets of growth conditions, K⁺ is always actively transported into the vacuole. Two possible mechanisms for active transport into the vacuole have been proposed, a 1:1 K⁺-H⁺ antiport (Hassidim et al., 1990) and the vacuolar K⁺-dependent, H⁺-transporting inorganic pyrophosphatase (Davies et al., 1992). Calculations of the thermodynamic feasibility of each of these indicates that both are possible mechanisms in barley leaf cells (results not shown). Therefore, it seems that salinization of barley leaf cells does not have any obvious effect on the direction or mechanism of active K⁺ transport at the tonoplast. This contrasts with K⁺-deprivation in barley roots which changes the direction of active K⁺ transport from into the vacuole in K⁺-replete conditions to into the cytosol in K⁺-deficiency (Walker et al., 1996). It was not possible to make similar calculations for active K⁺ transport at the plasma membrane of leaf cells because a_K in the apoplast of control and salinized leaves was not measured.

Walker et al. (1996) showed that cytosolic and vacuolar a_K in K⁺-replete barley root cells are about 80 mM and 120 mM, respectively, with little difference between epidermal and cortical cells. Comparison of these values with those for leaf cells from K⁺-replete, non-salinized plants (Table 2) shows that the a_K in the vacuoles of leaf cells is approximately twice that in the root cells, but the cytosolic values are similar. This indicates that cytosolic a_K is regulated to similar values in diferent cell types of barley while vacuolar a_K has different set points in root and leaf cells (see also Leigh, 2001). It would now be interesting to determine what regulatory processes operate on K⁺ transport at the plasma membrane and tonoplast to bring about this uniformity of cytosolic a_K, but differences in the vacuolar values. In particular, tonoplast transport must be under quite different control in root cells compared to leaf cells.

Finally, the work reported here will assist in attempts to use Na⁺-selective microelectrodes to measure the effect of salinity on cytosolic and vacuolar Na⁺ activities (Carden et al., 2001). Currently-available Na⁺ sensors show some sensitivity to K⁺, especially at Na⁺ activities between 1 and 10 mM (Carden et al., 2001). Therefore, knowledge of the values and behaviour of subcellular a_K in salinized plant cells is an important prerequisite for such studies. An approach combining the use of Na⁺- and K⁺-selective microelectrodes would allow the effects of salinity on cytosolic activities of these ions to be quantified and so allow hypotheses about the importance of cytosolic K⁺:Na⁺ ratio in salinity tolerance to be tested (Maathuis and Amtmann, 1999).

	Acknowledgements

 
The research was supported by grant B104CT960775 from the EU Biotechnology Programme 1994–1998. Rothamsted Research and Long Ashton Research Station are grant aided by the Biotechnology and Biological Sciences Research Council of the UK.

	References

Top Abstract Introduction Materials and methods Results Discussion References

 
Apse MP, Aharon GS, Snedden WA, Blumwald E. 1999. Salt tolerance conferred by overexpression of a vacuolar Na⁺/H⁺ antiport in Arabidopsis. Science 285, 1256–1258.[Abstract/Free Full Text]

Apse MP, Blumwald E. 2002. Engineering salt tolerance in plants. Current Opinion in Biotechnology 13, 146–150.[CrossRef][Web of Science][Medline]

Bertl A, Blumwald E, Coronado R, et al. 1992. Electrical measurements on endomembranes. Science 258, 873–874.[Free Full Text]

Carden DE, Diamond D, Miller AJ. 2001. An improved Na⁺-selective microelectrode for intracellular measurements in plant cells. Journal of Experimental Botany 52, 1353–1359.[Abstract/Free Full Text]

Cuin TA, Miller AJ, Laurie SA, Leigh RA. 1999. Nitrate interference with potassium-selective microelectrodes. Journal of Experimental Botany 50, 1709–1712.[Abstract/Free Full Text]

Davies JM, Poole RJ, Rea PA, Sanders D. 1992. Potassium transport into plant vacuoles energized directly by a proton-pumping inorganic pyrophosphatase. Proceedings of the National Academy of Sciences, USA 89, 11701–11705.[Abstract/Free Full Text]

Flowers TJ, Hajibagheri MA. 2001. Salinity tolerance in Hordeum vulgare: ion concentrations in root cells of cultivars differing in salt tolerance. Plant and Soil 231, 1–9.[CrossRef][Web of Science]

Flowers TJ, Yeo AR. 1995. Breeding for salinity resistance in crop plants: Where next? Australian Journal of Plant Physiology 22, 875–884.[Web of Science]

Fricke W. 1997. Cell turgor, osmotic pressure and water potential in the upper epidermis of barley leaves in relation to cell location and in response to NaCl and air humidity. Journal of Experimental Botany 48, 45–58.[Abstract/Free Full Text]

Fricke W, Hinde PS, Leigh RA, Tomos AD. 1995. Vacuolar solutes in the upper epidermis of barley leaves. Intercellular differences follow patterns. Planta 196, 40–49.[Web of Science]

Fricke W, Leigh RA, Tomos AD. 1994. Concentrations of inorganic and organic solutes in extracts from individual epidermal, mesophyll and bundle-sheath cells of barley leaves. Planta 192, 310–316.[Web of Science]

Fricke W, Leigh RA, Tomos AD. 1996. The intercellular distribution of vacuolar solutes in the epidermis and mesophyll of barley leaves changes in response to NaCl. Journal of Experimental Botany 47, 1413–1426.[Abstract/Free Full Text]

Fry CH, Hall SK, Blatter LA, McGuigan JAS. 1990. Analysis and presentation of intracellular measurements obtained with ion-selective microelectrodes. Experimental Physiology 75, 287–299.

Greenway H. 1962. Plant responses to saline substrates. II. Chloride, sodium and potassium uptake and translocation in young plants of Hordeum vulgare during and after a short sodium chloride treatment. Australian Journal of Biological Sciences 15, 39–57.

Hassidim M, Braun Y, Lerner HR, Reinhold L. 1990. Na⁺/H⁺ and K⁺/H⁺ antiport in root membrane vesicles isolated from the halophyte Atriplex and the glycophyte cotton. Plant Physiology 94, 1795–1801.[Abstract/Free Full Text]

Karley AJ, Leigh RA, Sanders D. 2000. Where do all the ions go? The cellular basis of differential ion accumulation in leaf cells. Trends in Plant Science 5, 465–470.[CrossRef][Web of Science][Medline]

Leigh RA. 2001. Potassium homeostasis and membrane transport. Journal of Plant Nutrition and Soil Science 164, 193–198.[CrossRef]

Leigh RA, Tomos AD. 1993. Ion distribution in cereal leaves—pathways and mechanisms. Philosophical Transactions of the Royal Society of London, Series B 341, 75–86.[CrossRef]

Leigh RA, Wyn Jones RG. 1984. A hypothesis relating critical potassium concentrations for growth to the distribution and functions of this ion in the plant cell. New Phytologist 97, 1–13.

Lubin M, Ennis HL. 1964. On the role of intracellular potassium in protein synthesis. Biochimica et Biophysica Acta 80, 614–631.[Medline]

Maathuis FJM, Amtmann A. 1999. K⁺ nutrition and Na⁺ toxicity: the basis of cellular K⁺/Na⁺ ratios. Annals of Botany 84, 123–133.[Abstract/Free Full Text]

Miller AJ, Cookson SJ, Smith SJ, Wells DM. 2001. The use of microelectrodes to investigate compartmentation and the transport of metabolized inorganic ions in plants. Journal of Experimental Botany 52, 541–549.[Abstract/Free Full Text]

Mühling KH, Läuchli A. 2000. Light-induced pH and K⁺ changes in the apoplast of intact leaves. Planta 212, 9–15.[CrossRef][Web of Science][Medline]

Robinson RA, Stokes RH. 1959. Electrolyte solutions. London: Butterworths.

Storey R, Pitman MG, Stelzer R, Carter C. 1983. X-ray microanalysis of cells and cell compartments of Atriplex spongiosa. I. Leaves. Journal of Experimental Botany 34, 778–794.[Abstract/Free Full Text]

Walker DJ, Black CR, Miller AJ. 1998. Role of cytosolic potassium and pH in the growth of barley roots. Plant Physiology 118, 957–964.[Abstract/Free Full Text]

Walker DJ, Leigh RA, Miller AJ. 1996. Potassium homeostasis in vacuolate plant cells. Proceedings of the National Academy of Sciences, USA 93, 10510–10514.[Abstract/Free Full Text]

Walker DJ, Smith SJ, Miller AJ. 1995. Simultaneous measurement of intracellular pH and K⁺ or NO₃^– in barley roots using triple-barreled, ion-selective microelectrodes. Plant Physiology 108, 743–751.[Abstract]

Yeo AR. 1981. Salt tolerance in the halophyte Suaeda maritima L. Dum: intracellular compartmentation of ions. Journal of Experimental Botany 32, 487–497.[Abstract/Free Full Text]

CiteULike    Connotea    Del.icio.us    What's this?

This article has been cited by other articles:

				V. Perez, T. Wherrett, S. Shabala, J. Muniz, O. Dobrovinskaya, and I. Pottosin Homeostatic control of slow vacuolar channels by luminal cations and evaluation of the channel-mediated tonoplast Ca2+ fluxes in situ J. Exp. Bot., October 1, 2008; (2008) ern225v1. [Abstract] [Full Text] [PDF]

				Z. Chen, S. Shabala, N. Mendham, I. Newman, G. Zhang, and M. Zhou Combining Ability of Salinity Tolerance on the Basis of NaCl-Induced K+ Flux from Roots of Barley Crop Sci., July 1, 2008; 48(4): 1382 - 1388. [Abstract] [Full Text] [PDF]

				T. A. Cuin, S. A. Betts, R. Chalmandrier, and S. Shabala A root's ability to retain K+ correlates with salt tolerance in wheat J. Exp. Bot., July 1, 2008; 59(10): 2697 - 2706. [Abstract] [Full Text] [PDF]

				Z. Chen, T. A. Cuin, M. Zhou, A. Twomey, B. P. Naidu, and S. Shabala Compatible solute accumulation and stress-mitigating effects in barley genotypes contrasting in their salt tolerance J. Exp. Bot., December 1, 2007; 58(15-16): 4245 - 4255. [Abstract] [Full Text] [PDF]

				Z. Chen, I. I. Pottosin, T. A. Cuin, A. T. Fuglsang, M. Tester, D. Jha, I. Zepeda-Jazo, M. Zhou, M. G. Palmgren, I. A. Newman, et al. Root Plasma Membrane Transporters Controlling K+/Na+ Homeostasis in Salt-Stressed Barley Plant Physiology, December 1, 2007; 145(4): 1714 - 1725. [Abstract] [Full Text] [PDF]

				A. Gobert, S. Isayenkov, C. Voelker, K. Czempinski, and F. J. M. Maathuis The two-pore channel TPK1 gene encodes the vacuolar K+ conductance and plays a role in K+ homeostasis PNAS, June 19, 2007; 104(25): 10726 - 10731. [Abstract] [Full Text] [PDF]

				A. Rodriguez-Navarro and F. Rubio High-affinity potassium and sodium transport systems in plants J. Exp. Bot., March 1, 2006; 57(5): 1149 - 1160. [Abstract] [Full Text] [PDF]

				W. Fricke, G. Akhiyarova, W. Wei, E. Alexandersson, A. Miller, P. O. Kjellbom, A. Richardson, T. Wojciechowski, L. Schreiber, D. Veselov, et al. The short-term growth response to salt of the developing barley leaf J. Exp. Bot., March 1, 2006; 57(5): 1079 - 1095. [Abstract] [Full Text] [PDF]

				P. Lobit, M. Genard, P. Soing, and R. Habib Modelling malic acid accumulation in fruits: relationships with organic acids, potassium, and temperature. J. Exp. Bot., January 1, 2006; 57(6): 1471 - 1483. [Abstract] [Full Text] [PDF]

				T. A. Cuin and S. Shabala Exogenously Supplied Compatible Solutes Rapidly Ameliorate NaCl-induced Potassium Efflux from Barley Roots Plant Cell Physiol., December 1, 2005; 46(12): 1924 - 1933. [Abstract] [Full Text] [PDF]

				R. R. Lew Osmotic Effects on the Electrical Properties of Arabidopsis Root Hair Vacuoles in Situ Plant Physiology, January 1, 2004; 134(1): 352 - 360. [Abstract] [Full Text] [PDF]

				S. SHABALA Regulation of Potassium Transport in Leaves: from Molecular to Tissue Level Ann. Bot., November 1, 2003; 92(5): 627 - 634. [Abstract] [Full Text] [PDF]

				S. J. Halperin and J. P. Lynch Effects of salinity on cytosolic Na+ and K+ in root hairs of Arabidopsis thaliana: in vivo measurements using the fluorescent dyes SBFI and PBFI J. Exp. Bot., September 1, 2003; 54(390): 2035 - 2043. [Abstract] [Full Text] [PDF]

This Article Abstract FREE Full Text (PDF) E-letters: Submit a response Alert me when this article is cited Alert me when E-letters are posted Alert me if a correction is posted Services Email this article to a friend Similar articles in this journal Similar articles in ISI Web of Science Similar articles in PubMed Alert me to new issues of the journal Add to My Personal Archive Download to citation manager Search for citing articles in: ISI Web of Science (50) Request Permissions Disclaimer Google Scholar Articles by Cuin, T. A. Articles by Leigh, R. A. Search for Related Content PubMed PubMed Citation Articles by Cuin, T. A. Articles by Leigh, R. A. Agricola Articles by Cuin, T. A. Articles by Leigh, R. A. Social Bookmarking          What's this?

Online ISSN 1460-2431 - Print ISSN 0022-0957

Copyright © 2005 Society for Experimental Biology

Oxford Journals Oxford University Press

• Site Map
• Privacy Policy
• Frequently Asked Questions

Other Oxford University Press sites: Oxford University Press Oxford Journals China Oxford Journals Japan American National Biography Booksellers' Information Service Children's Fiction and Poetry Children's Reference Corporate & Special Sales Dictionaries Dictionary of National Biography Digital Reference English Language Teaching Higher Education Textbooks Humanities International Education Unit Law Medicine Music Online Products Oxford English Dictionary Reference Rights and Permissions Science School Books Social Sciences Very Short Introductions World's Classics