JXB Advance Access originally published online on March 12, 2004
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Journal of Experimental Botany, Vol. 55, No. 398, pp. 939-949, April 1, 2004
© 2004 Oxford University Press
Plants and the Environment |
Alkali grass resists salt stress through high [K+] and an endodermis barrier to Na+
Received 28 November 2002; Accepted 11 November 2003
1 Institute of Plant Physiology and Ecology, Shanghai Institutes of Biological Sciences, Chinese Academy of Sciences, 300 Fenglin Road, Shanghai, 200032, PR China
2 Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, 39 East Beijing Road, Nanjing 210008, PR China
3 College of Life Science, LanZhou University, LanZhou 730000, PR China
* To whom correspondence should be addressed. Fax: +86 21 6404 2385. E-mail: zstressc{at}online.sh.cn
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Abstract |
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In order to understand the salt-tolerance mechanism of alkali grass (Puccinellia tenuiflora) compared with wheat (Triticum aestivum L.), [K+] and [Na+] in roots and shoots in response to salt treatments were examined with ion element analysis and X-ray microanalysis. Both the rapid K+ and Na+ influx in response to different NaCl and KCl treatments, and the accumulation of K+ and Na+ as the plants acclimated to long-term stress were studied in culture- solution experiments. A higher K+ uptake under normal and saline conditions was evident in alkali grass compared with that in wheat, and electrophysiological analyses indicated that the different uptake probably resulted from the higher K+/Na+ selectivity of the plasma membrane. When external [K+] was high, K+ uptake and transport from roots to shoots were inhibited by exogenous Cs+, while TEA (tetraethylammonium) only inhibited K+ transport from the root to the shoot. K+ uptake was not influenced by Cs+ when plants were K+ starved. It was shown by X-ray microanalysis that high [K+] and low [Na+] existed in the endodermal cells of alkali grass roots, suggesting this to be the tissue where Cs+ inhibition occurs. These results suggest that the K+/Na+ selectivity of potassium channels and the existence of an apoplastic barrier, the Casparian bands of the endodermis, lead to the lateral gradient of K+ and Na+ across root tissue, resulting not only in high levels of [K+] in the shoot but also a large [Na+] gradient between the root and the shoot.
Key words: Cs, endodermis, electrophysiological analysis, K+/Na+ selectivity, Puccinellia tenuiflora, salt tolerance, TEA, wheat, X-ray microanalysis.
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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High salinity is one of the most important environmental stresses impeding crop growth. It severely reduces agricultural yields and productivity (Greenway and Munns, 1980; Epstein et al., 1980; Flowers and Yeo, 1995). A key factor limiting plant growth in the case of salt stress, besides decreased water potential, is excessive Na+, a harmful mineral element not required by most glycophytes for normal growth (Niu et al., 1995). High Na+ tissue content is, therefore, often considered as the most critical factor responsible for salt toxicity in non-halophytes (Greenway and Munns, 1980; Niu et al., 1995).
At the level of individual cells, one of the most damaging consequences of salt stress is an influx of Na+ and a decrease of [K+] in plant tissues. K+ plays a key role in several physiological processes, such as osmotic regulation, protein synthesis, and enzyme activation. The substitution of K+ by Na+ may lead to nutritional imbalance. The mechanisms of Na+ influx are not very clear yet, but there is evidence that low affinity non-selective channels or Na+ permeability properties of the K+ transport system (e.g. LCT1 and HKT1) can facilitate Na+ influx (Amtmann and Sanders, 1999; Maathuis and Amtmann, 1999; Uozumi et al., 2000; Amtmann et al., 2001; Rus et al., 2001). The competition between Na+ and K+ results from the similarity of their hydrated ionic radii: sodium (1.65
2.053 Å) and potassium (2.3502.66 Å) (Biggin et al., 2001). Potassium starvation regularly accompanies sodium toxicity (Flowers and Läuchli, 1983). The ideal plant response to salt stress is to maintain low cytosolic [Na+] and high cytosolic [K+ ]. Minimal initial Na+ entry should, consequently, be very important for plant salt tolerance. Thus the discrimination to ions of transporters and channel proteins in roots is quite important, and is considered to be an index of salt resistance (Guillermo et al., 2001). Alternatively, sodium compartmentation and sodium extrusion could also lead to low cytosolic [Na +]. These molecular mechanisms have been reviewed in detail in some recent papers and will not be discussed further here (Blumwald et al., 2000; Zhu, 2002; Tester and Davenport, 2003).
At the level of the whole plant, plants have solute exclusion mechanisms to maintain low [Na+] in shoots under salt stress; these contribute to the salt tolerance of the whole plant, but not at the level of individual cells and they are based on anatomical rather than molecular mechanisms. Casparian bands in plant roots contain both aliphatic and aromatic suberins (Schreiber et al., 1999). Schreiber’s group suggest that the Casparian bands are fairly impermeable to ions and to high molecular weight polar solutes, but may allow some passage of water and small solutes (Schreiber et al., 1999). Charged solutes are effectively excluded by the presence of endodermal Casparian bands in solute transport competition tests with PTS (3-hydroxy-5,8,10-pyrene-trisulphonate) (Steudle, 2000). The endodermal tissue acts as an efficient barrier to ions released into the apoplast of the xylem, and this allows root pressure to build up. Sodium compartmentation in the whole plant, especially the Na + gradient between the root and the shoot, is the result of the solute transport mechanism (Watson et al., 2001). It is suggested that it contributes to the salt tolerance of plants and is as important as the other molecular mechanisms. Recent research indicated that SOS1, a putative plasma membrane Na+/H+ antiporter, could control long-distance Na+ transport in plants (Shi et al., 2000, 2002). For further understanding of whole plant tolerance, more knowledge of cell-specific transport processes and the consequences of the manipulation of transporters in specific cell types is required.
Most monocotyledonous crop species are glycophytes, which are sensitive to salinity. The deficiency of good model plants is a big problem when studying salt tolerance mechanisms in monocotyledonous crops. However, in the saline meadows and marshes of Central Asia, a graminaceous grass, Puccinellia tenuiflora (so-called ‘alkali grass’ in Chinese), is a kind of monocotyledonous halophyte. Unlike other graminaceous crop such as wheat (Gramineae), Puccinellia tenuiflora is strongly salt resistant. Anatomical and ecological studies of this plant have been reported, but there is little knowledge on which of the above mechanisms are responsible for its salt resistance (Wang et al., 1994; Zhu et al., 2001). Several functional genes in alkali grass have been cloned that show highly conserved sequences with rice or wheat (data not shown). Alkali grass also shares a similar life history and growth condition with rice. Tissue culture and gene manipulation is not difficult in alkali grass. These physiological characteristics of alkali grass show that it may be a good contrast and model plant with which to study salt tolerance mechanisms in monocotyledonous crops. In this paper, research on the response of alkali grass to salt will contribute to an enhanced understanding on salt resistance of Graminaceous crops.
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Materials and methods |
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Plant material and growth conditions
Seeds of alkali grass Puccinellia tenuiflora and wheat (Triticum aestivum L. var. Qi 4185) were germinated at 28 °C. Seedlings were grown in 1/2 strength Hoagland solution at a photon flux density of 350
400 µmol m–2 s–1 with 12/12 h day/night cycle at 28 °C in the phytotron. Plants at the three leaf stage were treated with different conditions. The details of treatments are indicated in the legends and notations of Figs 1 and 2 in the Results.
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Na+ and K+ determination
The shoots and roots of the plants were rinsed with deionized water three times, dried with filter paper, then dried at 80 °C to a constant weight. 0.1 g dry powder samples were then extracted with 5 ml 4 M HCl at 37 °C overnight to release the free cations. The supernatants of the extracts, after centrifugation at 10 000 g for 10 min, were diluted and Na + and K+ determined with a Shimadzu AA-680 atomic absorption/flame spectrophotometer.
Plasma membrane isolation and purification
Plasma membrane was purified from young roots of wheat and alkali grass by partitioning microsomes in an aqueous dextran–polyethylene glycol two-phase system (Larsson et al., 1987).
Channel recordings
Planar lipid bilayers (PLBs) were prepared according to Li et al. (1996). PLBs were made by dispersing 25 mg L-
-lecithin IV-S (Sigma) and 8 mg cholesterol (Sigma) in 1 ml decane then brushing it past a hole of 0.3–0.5 mm diameter in the Teflon-coated separation wall between the two chambers. Adding cholesterol made the artificial bilayers more similar to plant plasma membranes and enhanced the stability of PLBs. Channel activity was detected in a solution consisting of 100 mmol l–1 KCl or NaCl, 1 µmol l–1 CaCl2, and 5 mmol l–1 MES/TRIS pH 7.0. Most of the plasma membrane vesicles obtained by aqueous two-phase partitioning were right-side out vesicles, and the cis- and trans-chambers were represented by the outside and inside of cells, respectively, after the vesicles were incorporated into PLBs. A reference electrode was in a trans -chamber. The current and voltage characteristics of plasma membrane were recorded by a single electrode voltage clamp amplifier, CEZ-3100 and monitored by oscilloscope. Current moving from the cis to trans was positive. From the tested Erev and the following Goldman–Hodgkin–Katz (GHK) function, the ratio of PK/PNa was obtained. It was taken as the filter coefficient of K+ and Na+.
where R is the gas constant, T is the absolute temperature, F is the Faraday constant, Z is the valency of ions, RT/ZF=25.26 mV when the temperature is 20 °C, PK, PNa is the permeability of K+ and Na+, and [ ]cis, [ ]trans, is the ion concentration of the cis -chamber and the trans-chamber, respectively.
X-ray microanalysis
Roots of seedlings at the three leaf stage from different treatments were washed with distilled water three times. The harvested root segments, including the tip and 1 cm or more of the root, were dipped in 5% agar, inserted to a depth of 1.0 cm in a copper holder, and immediately sliced free-hand with a razor blade to get transverse sections, and then frozen in liquid nitrogen. The samples were freeze-dried, carbon coated in a high vacuum sputter coater, and stored in a desiccator (Van Steveninck and Van Steveninck, 1991). Samples were analysed in a JSM-6300 scanning electron microscope equipped with an energy-dispersive X-ray detector (Sigma) (Tomos et al., 1994). Counts per second of [K+], [Na+], and [Cs+] were measured in roots from the six different treatments: (solution concentration of K+, Na+ and Cs+ were replaced by 3, 3, 0; 3, 200, 0; 3, 200, 10; 0.02, 3, 0; 0.02, 200, 0; and 0.02, 200, 10). Six tissues, i.e. epidermal cells, exodermal intercellular space, exodermal cells, cortical cells, endoderm cells, and the stelar parenchyma in each root transverse section were analysed. More than three transverse sections of each treatment were observed and three location spots of the same tissue of each section were analysed. Both Map-scan, and line-scan were done.
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Results |
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Main differences in K+ and Na+ accumulation between alkali grass and wheat under salt stress
The seedling roots of alkali grass grown in 1/2 strength Hoaglands culture solution (with 3 mM Na+ and 3 mM K+ inside) had a [K+] 2.72 times that of wheat grown in the same conditions, and had a K+/Na+ ratio of 1.64 compared with 0.37 for wheat (Fig. 1a, b). The ratio decreased respectively in alkali grass and wheat when NaCl concentration in the culture solution increased to 25, 100, 200, and 300 mM for 8 d (Fig. 1 b). The [K+] in alkali grass for these treatments were 2.7–4 times higher than those in wheat treated in the same way. With the increase of [NaCl] in culture solution, the differences of [Na+] between roots and shoots were enhanced in alkali grass, while they declined in wheat (Fig. 1c). Wheat wilted and could not survive in the 400 mM NaCl treatment; by contrast, alkali grass grew well. K+/Na+ selectivity (SA) of the roots was defined as the quotient of the [Na+]/[K+] in the medium divided by the [Na+]/[K+] in the root ( Pitman, 1984; Yeo and Flowers, 1986; Flowers and Yeo, 1988). After long-term exposure to elevated NaCl concentrations, the SA values of alkali grass roots became substantially greater (higher K+ selection) than those of wheat (Fig. 1d).
K+ and Na+ uptake in alkali grass under salt shock and the K+ channel inhibitor Cs+
[Na+] and [K+] in the roots of alkali grass increased synchronously in the first h after 200 mM NaCl treatment, but no large change was seen in the shoot (Fig. 2). Cs+ is an inhibitor of the inward-rectifying K+ channel. In the 10 mM Cs+ plus 200 mM NaCl treatment, [K+] was markedly lower than in the Cs +-free plus 200 mM NaCl treatment, although the difference in [Na+] between these two treatments was minimal (Fig. 3). A lower ratio of [K+]/[Na+] in the alkali grass root resulted when Cs+ was present with salt (Fig. 4). Alkali grass treated with Cs + became sensitive to salt and could not survive in 200 mM NaCl.
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Selective permeability of plasma membranes from alkali grass and wheat
PLBs were made successfully and remained stable for at least 20 min. The I-V relationship of the PLBs was detected without adding plasma membranes. The PLBs kept a constant membrane resistance (
10G
) in the voltage range between –100 mV and +100 mV. The membrane vesicles were put into a cis-chamber. Figure 5a shows single-channel signal recordings of alkali grass and wheat within 0–40 mV, with a constant conductance of about 45 pS, respectively. This type of channel is similar to those detected in plasma membranes of tobacco callus (42 pS; Li et al., 1996), and barley protoplasts (45 pS; Wegner and De Boer, 1997). The relationship of I-V exhibited linearity in the range of 0–40 mV in wheat, as indicated by Fig. 5b. When the holding voltage was positive, the values of the current pulse of the channel in an opening situation increased with the enhancement of the holding voltage. When the patch voltage was negative, the current pulse decreased dramatically, which indicated that this type of channel had a character of inward-rectifying. The inward current was almost completely blocked by the addition of 10 mmol l–1 TEA, commonly employed as a blocker of K+ channels (Fig. 5c).
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The relationships of I-V in 100 mmol l–1 KCl solution of plasma membranes from alkali grass and wheat were measured by rapidly setting different holding voltages as soon as multi-channel signals appeared in the planar lipid bilayer. Multi-channel signals were selected as they could exhibit the conductance of whole plasma membranes. Multi-channel signals are defined here as total current through the bilayer after subtraction of current measured before vesicle fusion. The relative currents were recorded (Fig. 6). The linear equations describing these relationships in alkali grass and wheat were y=1.5178x–0.2143, and y=0.7642x+0.7788, respectively. The slopes of the equations for the membranes of alkali grass and wheat were 1.5179 and 0.7642. The fact that the slope of the equation for alkali grass was much steeper than the one for wheat shows that the permeability to K+ of the plasma membrane from alkali grass was markedly higher than that from wheat.
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100 mmol l–1 KCl solution in the trans -chamber was replaced by 100 mmol l–1 NaCl. Using the procedure described above, the equations of the relationship of Im and Vm with asymmetric solutions of KCl and NaCl for plasma membranes from alkali grass and wheat were derived (Fig. 7). The reverse membrane voltages (Erev) were obtained from linear regression analysis of the equations for alkali grass and wheat. The ratio of PK+/PNa+ for alkali grass was 4.96 and for wheat was 4.05. This ratio was extracted using the Goldman–Hodgkin–Katz (GHK) functions. The K+/Na+ selectivity of the membrane of alkali grass was higher than that for wheat, suggesting an explanation for the differences in K+ and Na+ uptake between the two species.
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Comparison between the K+, Na + accumulations with different levels of K+ and channel inhibitors in alkali grass
The alkali grass seedlings were treated with different levels of CsCl (2 mM, 10 mM, 20 mM) and different levels of K+ (3 mM and 20 µM) in saline (200 mmol l–1) culture solution. The results showed that the inhibition by Cs+ of K+ uptake by seedlings depended on the K+ level in the solution (Fig. 8). No large inhibition by Cs+ on K+ uptake could be observed in the seedlings treated with low levels of K+, regardless of the level of Cs+ used, while the inhibition increased stepwise when [Cs+] was increased in the high [K+] treatments. The inhibition by 20 mM CsCl was so strong that the [K+] of roots in 3 mM K + solution was decreased to a similar [K+] as the roots grown in 20 µM K+ solution.
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TEA (tetraethylammonium), another specific K+- channel inhibitor, was used to inhibit K+ uptake of the seedlings grown in 3 mM K+ plus 200 mmol NaCl and 20 µM K + plus 200 mmol NaCl treatments, respectively. TEA only resulted in reduced [K+] in shoots of seedling grown at high K+. In addition to reducing [K+] of the shoots, TEA reduced [Na+] of both roots and shoots in seedlings grown in the low K+ treatments (Fig. 9a, b). TEA distinguished the ions selectivity and compartmentalization functions of the high-affinity K+ transporter from that of the low-affinity one.
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X-ray microanalysis of root transverse sections of alkali grass
Transverse sections of the roots of alkali grass seedlings were scanned by X-ray micro-analysis, beginning with the outermost tissues and proceeding to the middle ones in the order: epidermal cells, exodermis intercellular space, exodermis cells, cortical cells, endoderm cells, and stelar parenchyma (Fig. 10). Figure 11 shows a typical spectrum of the X-ray microanalysis. Many of these spectra were transformed to data by the professional software in the computer of JSM-6300. Counts per second for [K+], [Na+], [Ca2+], and [Cs+] of the six treatments 3, 3, 0 mM [K+], [Na+], [Cs+ ]; 3, 200, 0; 3, 200, 10; 0.02, 3, 0; 0.02, 200, 0; and 0.02, 200, 10 are summarized in Table 1.
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In the roots of the salt-free treatments 3, 3, 0 mM [K+], [Na+], [Cs+] and 0.02, 3, 0, K+ levels increased in a gradient from the outer root tissues to the middle ones (Table 1; Fig. 12). On the other hand, [Na+] was generally lower in the mid-root tissues compared with the outermost ones (Table 1; Fig. 13b, d). The highest ratio of [K+]/[Na+] was in the cortical cells and the xylem (Fig. 10), and both K+ and Na+ were asymmetrically distributed. In the salt-stress treatment, 3, 200, 0 mM, [Na+] increased markedly, but K+ did not decrease and was comparable to the 3, 3, 0 mM treatment. [K +] in the xylem was still higher than that in other tissues and [Na+] in the xylem was relatively low. The Cs+ treatments, 3, 200, 10 and 0.02, 200, 10 mM decreased [K+] and increased [Na+] in all tissues tested, particularly in the xylem (Table 1; Fig. 13h). Thus, lower ratios of [K+]/[Na+ ] resulted, with the lowest in stelar cells and the highest in cortical cells (Fig. 10). The results are interpreted as evidence that alkali grass has a relatively strong blocking function to avoid penetration of Na+; Cs+, as expected, inhibited K+ uptake and transport to the xylem (Figs 12, 13h).
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K+ enrichment in the xylem declined a little under potassium starvation in the 0.02, 3, 0 mM treatment compared with 3, 3, 0 mM (Fig. 12; Table 1); and this decline was greater under salt stress (0.02, 200, 0 mM treatment). The decline in K+ enrichment was accentuated as more Cs+ appeared in the root tissues inhibiting K+ uptake as shown in the 0.02, 200, 10 mM treatment.
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Discussion |
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Potassium is an essential element for living cells and an absolute requirement for many cellular functions such as osmotic regulation, protein synthesis, and enzyme activation (Evans and Wildes, 1971). In the sos mutants of Arabidopsis, the level of salt tolerance as measured by root growth correlates closely with tissue K+ content (Zhu et al., 1998). Several reports from studies on plant cell cultures and yeast cells have also suggested the importance of K+ nutrition in salt tolerance (Watad et al., 1991; Gaxiola et al., 1992). The high level of K+ and the strong salt tolerance in alkali grass compared with wheat are consistent with the key role of K+ nutrition in plant salt tolerance. A higher K+ uptake under normal and saline conditions showed in alkali grass, which indicated that a high K+/Na+ selectivity of potassium transport systems might be critical in plant salt tolerance. To confirm this, more direct evidence and the research to integrate the knowledge from molecular biology into whole plants is necessary, since the ion transport mechanisms of higher plants involve many transport proteins with very complex interactions.
K+ channel blockers are potent tools for the study of the physiological functions of potassium transport systems. Both TEA and Cs + are potassium channel blockers, but they act on different channels (Khodakhah et al., 1997; Ichida et al., 1997). As shown in these results, Cs+ inhibited K+ uptake and translocation from roots to shoots when plants were exposed to high [K+] medium, while only K+ translocation from roots to shoots was inhibited by TEA (Fig. 9a). However, both K+ and Na+ translocation were inhibited by TEA when plants were exposed to low [K+] medium (Fig. 9b). This is evidence for the involvement of low-affinity channels in the K+ uptake of alkali grass. TEA-sensitive channels function in K+ transport from the root to the shoot, while Cs+-sensitive channels appear to be involved in K+ uptake by the root and its transportation. These various K+ channel proteins had different distributions and functions in the roots of alkali grass. High-affinity K+ transport systems are supposed to be induced and function in K+ uptake when plants are exposed to low [K+] medium (Schachtman and Schroeder, 1994). K+ uptake decreased and Na+ content increased in the root of alkali grass exposed to low [K+] medium compared with the treatments of high [K+] medium adjusted to have the same salt stress. It suggests that the high-affinity potassium transport system may have a low K+/Na+ selectivity. In summary, these results show that a low affinity system was the main path for K+ uptake, and that the decline of salt tolerance under low K+ conditions might have resulted from increased Na+ entrance through the high affinity system.
The management of Na+ movements within the plant requires specific cell types in specific locations. Many reports have shown that solute transportation is different from water transport. Solutes such as Na+, K+, Ca2+, Mg2+, and ABA moved freely in the apoplast of roots, and need to pass the Casparian bands of the endodermis to reach the apoplast of the xylem. Solute transport into the xylem is controlled by the plasma membrane of endodermal cells (Peterson et al., 1993; Steudle, 2000; Kuhn et al., 2000). X-ray analysis of roots of alkali grass under salt stress showed that Na+ was distributed mainly in the intercellular space of the endoderm while K+ was concentrated in the cells and xylem to function in osmotic regulation (Fig. 12). The asymmetric distribution of K+ and Na+ changed relatively, even when channel block inhibitors were used, which indicated the barrier and filter functions of endodermal cells. The management of Na+ movements within the plant results from specific cell types in specific locations with the plant catalysing transportation in a co-ordinated manner. To understand complex, whole-plant adaptations to salinity further, more information is required about cell-specific transport processes and the consequences of the manipulation of transporters in specific cell types, such as endodermal cells.
In conclusion, Fig. 14 is proposed as a model to explain the mechanism resulting in K+/Na+ selectivity of plant. It includes an apoplastic and a symplastic path of K+ and Na+ penetration into the root. It also indicates various ion channels and transporters within cell membranes. The high K+/Na+ selectivity of some low-affinity K+ transporters located in the plasma membrane of root cells may endow alkali grass with high salt tolerance. Their presence allowed the plant to maintain high [K+] and low [Na+] in the cells thus withstanding high [Na+] in the cell environment. The Casparian band in the endoderm blocked the apoplastic path of Na+ entrance, enhancing the function of low-affinity K+ transporters to increase the [Na+] gradient between the root and shoot. Because alkali grass is closely related to many crop species, this research on its salt-tolerance pattern may help to enhance the salt-tolerance capacity of graminaceous plants by using transgenetic methods in the future.
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Acknowledgements |
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This research was supported by the National Key Basic Research Special Fund of China (G1999011700) and the Key Basic Research Special Fund of CAS (KSCXZ-SW-116). We thank Dr David Lane for his advice.
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References |
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