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Plant Physiol. (1999) 119: 165-172 Myo-Inositol-Dependent Sodium Uptake in Ice Plant1
Department of Biochemistry (D.E.N., M.K., H.J.B.), Department of Plant Sciences (H.J.B.), and Department of Molecular and Cellular Biology (H.J.B.), The University of Arizona, Tucson, Arizona 85721
In salt-stressed ice plants (Mesembryanthemum crystallinum), sodium accumulates to high concentrations in vacuoles, and polyols (myo-inositol, D-ononitol, and D-pinitol) accumulate in the cytosol. Polyol synthesis is regulated by NaCl and involves induction and repression of gene expression (D.E. Nelson, B. Shen, and H.J. Bohnert [1998] Plant Cell 10: 753-764). In the study reported here we found increased phloem transport of myo-inositol and reciprocal increased transport of sodium and inositol to leaves under stress. To determine the relationship between increased translocation and sodium uptake, we analyzed the effects of exogenous application of myo-inositol: The NaCl-inducible ice plant myo-inositol 1-phosphate synthase is repressed in roots, and sodium uptake from root to shoot increases without stimulating growth. Sodium uptake and transport through the xylem was coupled to a 10-fold increase of myo-inositol and ononitol in the xylem. Seedlings of the ice plant are not salt-tolerant, and yet the addition of exogenous myo-inositol conferred upon them patterns of gene expression and polyol accumulation observed in mature, salt-tolerant plants. Sodium uptake and transport through the xylem was enhanced in the presence of myo-inositol. The results indicate an interdependence of sodium uptake and alterations in the distribution of myo-inositol. We hypothesize that myo-inositol could serve not only as a substrate for the production of compatible solutes but also as a leaf-to-root signal that promotes sodium uptake.
Current strategies for improving tolerance to sodium stress,
whether based on breeding or transformation, rely primarily on the
production of low-Mr solutes and on
enhancing radical-scavenging enzyme systems (Tarczynski et al., 1993 In the case of exclusion, a plasma membrane sodium/proton antiporter
has yet to be found and a functionally homologous vacuolar Na+/H+-antiporter,
important for compartmentation, has only been described physiologically
(Barkla and Blumwald, 1991 We report that a portion of the pathway for sodium transport from root
to leaf involves an interaction between myo-inositol and
sodium, i.e. we suggest that myo-inositol acts as a
facilitator of sodium uptake and long-distance transport. The results
extend our previous studies of the expression of genes for the inositol biosynthetic pathway, INPS
(myo-inositol-1-phosphate
synthase, EC 5.5.1.4), IMP
(myo-inositol
monophosphatase), and IMT
(myo-inositol O-methyltransferase, EC 2.1.1.129;
Vernon and Bohnert, 1992 Myo-inositol and its derivatives are typically examined with
regard to cell signaling and membrane biogenesis, but they also participate in responses to salinity in animals and plants. In animal
cells membrane transport of hexoses, including the action of SMIT, is
linked to sodium uptake. The physiological purpose seems to be for
myo-inositol to act as a compatible solute (Garcia-Perez and
Burg, 1991 A relationship between ion uptake and myo-inositol
biosynthesis in cell cultures was previously reported (Wood and Braun, 1961 We have characterized myo-inositol transport in the
salt-stressed ice plant (Mesembryanthemum crystallinum). The
results build on our previous findings (Vernon and Bohnert, 1992 Plant Growth Conditions
Protein Analysis Protein from leaf and root tissue was extracted directly in Laemmli buffer containing protease inhibitors (1 mM PMSF, 1 µg/mL leupeptin, and 1 µg/mL E-64). Bradford assays were used to determine protein, followed by protein separation on SDS-PAGE (Nelson et al., 1998a ). Protein was transferred to nitrocellulose by
electroblotting and detected using a 1:5000 dilution of primary
antibodies diluted in TBS buffer containing 1% Tween 20 and 1%
powdered milk. Goat anti-rabbit antibody conjugated to horseradish
peroxidase diluted 1:5000 in the same buffer was used to detect
the primary antibodies. Detection of the complex was by
chemiluminescence using ECL reagents (Amersham).
Collection of Phloem Exudate, Xylem Sap, and Measurement of Solutes The collection of phloem exudate was used according to the method of King and Zeevaart (1974). Side shoots bearing two leaf pairs of
4-week-old plants were excised 4 h after the start of the light
period. The cut surface was submerged in 2 mL of 10 mM
EDTA, pH 8.0, contained in liquid-scintillation vials. After a 2-h
incubation period to wash out solutes released directly at the cut
surface, the side shoots were placed in fresh medium for an additional
4 h. For xylem sap (extracellular sap) collection, side shoots
were placed in a pressure chamber (PMS Instrument Co., Corvallis, OR).
The chamber was slowly pressurized with nitrogen. Initial exudate from
the cut surface was discarded and exudate for sampling was collected.
Methods used for solute analysis have been described (Adams et al.,
1992, 1993, 1998).
Correlation of Myo-Inositol Synthesis and NaCl Accumulation The illustration in Figure 1 is based on immunocytology and solute measurements (Nelson et al., 1998a)
and relates the data of previous experiments (Ishitani et al., 1996;
Nelson et al., 1998a) to the hypothesis that we present here. In the
ice plant prior to NaCl treatment, de novo myo-inositol
synthesis seems to be cell autonomous, i.e. all cells are able to
synthesize myo-inositol, although INPS amounts vary between
cell types. This autonomy is lost in response to salt stress: following
NaCl treatment, INPS increases in leaf mesophyll tissue and decreases
in all parts of the root. Within the limits of detection by
immunoblotting and immunocytology, INPS seems to disappear completely
from the roots. Based on NaCl-induced increased translocation of
myo-inositol and ononitol through the phloem, Figure 1
points to the difference in myo-inositol synthesis between
the shoot and the root. The induction of INPS in leaf cells is
consistent with a role in supplying a substrate for pinitol, which
accumulates in the cytosol along with sodium in vacuoles of cells in
aerial tissues. The repression of INPS in roots (Nelson et al., 1998a)
was unexpected and did not fit a model in which INPS regulation would
solely provide the substrate for methylation reactions, suggesting the
possibility of myo-inositol acting as a shoot-to-root signal
for sodium uptake. A hydroponic system was used in the experiments
described here and showed a correlation between the presence of
myo-inositol in roots and sodium uptake into leaves.
Feedback Inhibition of Myo-Inositol Synthesis In yeast myo-inositol synthesis is feedback inhibited by exogenous myo-inositol (Culbertson et al., 1976; Ashburner and Lopes, 1995). Since NaCl treatment resulted
in the repression of INPS accumulation in roots (Nelson et al.,
1998a), we tested the effect of exogenous
myo-inositol on INPS amounts in seedling roots (Fig. 2). Myo-inositol at 5 to
10 mM completely repressed INPS expression (data not
shown), confirming that the NaCl-inducible INPS in the ice plant is
feedback inhibited by myo-inositol.
Synergy of NaCl and Myo-Inositol Treatment Because myo-inositol translocation to roots increased after salt stress, and since young seedlings have not yet developed the degree of NaCl tolerance exhibited by older plants (Cushman et al., 1990), we tested the effect of exogenous myo-inositol application to roots on NaCl accumulation in the leaves. Hydroponically grown seedlings were treated with combinations of NaCl and
myo-inositol, and leaves were harvested for solute analysis
after 3 d. Little sodium was found in the leaves of control plants
and in plants treated with 1 to 25 mM
myo-inositol (Fig. 3A, 10 mM). Treatment of seedlings with 100 mM NaCl
alone resulted in an increase in sodium in leaves. Finally, the
combination of NaCl and myo-inositol resulted in a higher
accumulation of sodium than the treatment with only NaCl. None of these
treatments altered the amount of leaf potassium in comparison to the
controls (Fig. 3B), indicating that the effect was specific to sodium.
From these data, the ratio of sodium to potassium was calculated (Fig.
3C). Simultaneous treatment with myo-inositol and NaCl
dramatically increased the ratio to a level similar to that in
sodium-treated, mature ice plants (Adams et al., 1992, 1998) and in
adapted tobacco cells (Binzel et al., 1988). In the ice plant the ratio
varied from 11 to 13 in leaves of treated plants, whereas in control
plants the ratio was 0.5. In the adapted tobacco cells the ratio ranged from 0.27 in control cells to 8.2 in cells adapted to 428 mM NaCl. When the data of Binzel et al. (1985) are
regressed to 100 mM NaCl, the expected ratio is near 2, similar to the ratio of 1.7 observed in ice plant seedlings treated
with 100 mM NaCl and myo-inositol. In other
unadapted glycophytes such ratios are typically <1 (Garcia et al.,
1997). The results show that myo-inositol treatment
converted intolerant seedlings to a physiological condition indicative
of more mature ice plants (Adams et al., 1998).
Titration of Myo-Inositol Next, the concentration of myo-inositol necessary to stimulate sodium accumulation was determined. A concentration of 100 µM caused an accumulation of sodium to a significantly higher level than the controls but no different from treatment with NaCl alone (Fig. 4). At 300 µM stimulation was significantly greater than both controls, but the effective concentration for stimulation of sodium uptake is likely lower because other synthetic pathways undoubtedly consume some of the exogenously applied myo-inositol.
Myo-Inositol Does Not Stimulate Growth Cell expansion could have diluted the effect of salt uptake, and an inositol-dependent stimulation of growth might lead to an increased accumulation of sodium. To determine whether myo-inositol stimulated seedling growth, plants were treated with 10 mM myo-inositol. The fresh weights of the roots and leaves were taken at the beginning of the experiment. After 3 d control and myo-inositol-treated plants were compared. During the 3-d period the fresh weight of control and stressed plants doubled (data not shown), indicating that myo-inositol did not stimulate sodium accumulation indirectly through a stimulation of growth. In older plants, such as those used for obtaining phloem and xylem contents (Nelson et al., 1998a; Table I),
salinity stress accelerates growth for several weeks (Adams et al.,
1998) and no significant reduction in xylem sap recovery was observed,
whereas xylem xylem is reduced when the plants switch from
C3 to CAM.
Stimulation of IMT Accumulation by Myo-Inositol It had been shown that ice plant seedlings are not salt tolerant and do not express the Imt1 gene or accumulate IMT protein following NaCl treatment as older plants do (Cushman et al., 1990; Vernon and Bohnert, 1992; Ishitani et al., 1996). Since
myo-inositol stimulated sodium uptake (Fig. 3), the effect
of myo-inositol on IMT accumulation was tested. In fact, the
addition of sodium and myo-inositol together caused the
accumulation of IMT in leaves (Fig. 5A)
and roots (Fig. 5B), converting the seedlings to a state that is
characteristic of older plants. The addition of either NaCl or
myo-inositol alone did not stimulate IMT, indicating a synergistic interaction between the compounds.
Myo-Inositol Stimulates the NaCl Induction of Polyol Accumulation To confirm the results of the protein analysis, the accumulation of leaf polyols was measured following treatment with two concentrations of NaCl and three concentrations of myo-inositol. In the absence of stress, the seedlings did not contain more total polyols until at least 10 mM myo-inositol was added (Fig. 6). In the absence of myo-inositol, there was no increase in polyol accumulation even under stress. Treatment with as low as 1 mM myo-inositol in the presence of 150 mM NaCl increased the amount of total polyols significantly and caused the seedlings to respond like mature plants.
Maintenance of the Sodium-to-Polyol Ratio Following NaCl treatment, ice plants establish a similar ratio of sodium to pinitol throughout their life cycle (Adams et al., 1998) with
values of approximately 100 in juvenile leaves (5 d), 76 in adult
leaves (35 d ), and 83 in adult leaves (61 d). The ratio of sodium to
total polyols (myo-inositol plus ononitol plus pinitol) was
determined for leaves of hydroponically grown 2-week-old seedlings
treated for 3 d (n = 5 for each treatment) in the
presence or absence of 10 mM myo-inositol, 100 mM NaCl, and 10 mM myo-inositol plus
100 mM NaCl. Control plants had a ratio of approximately
30, which became highly skewed following treatment by either
myo-inositol (7) or NaCl (120), and both compounds together
returned the ratio to near the control value (37). Furthermore, the
absolute amounts of NaCl and polyols increased equally, approximately 10-fold, from the control to the double-treated plants.
Extracellular Location of Myo-Inositol and Ononitol Sodium seems to enter the plant initially through the root apoplastic space. In maize, for example, sodium is detected in the xylem prior to its appearance in vacuoles of cortical cells (Frensch et al., 1992) and does so by passive movement. Similarly, apoplastic
movement of sodium has also been observed in rice, but wheat seems to
utilize another mechanism recognizable by a different potassium:sodium
discrimination (Garcia et al., 1997). In the ice plant,
myo-inositol is translocated to the root and this
facilitates sodium uptake. Myo-inositol may play an indirect role in sodium uptake by exerting its effect from the cytoplasm. Alternatively, if it were to be found in the extracellular space, it
may play a direct role. To test whether myo-inositol can be found extracellularly, side shoots were used to analyze xylem contents
(Nelson et al., 1998a). Side shoots were pressurized in a
pressure chamber and sap was collected. These samples may not contain
xylem sap exclusively, but, based on the absence of Suc, the samples
were not significantly contaminated by either phloem or cytoplasmic
contents of other cells (Table I). An expected large increase in sodium
following stress was observed and, in addition, a 10-fold increase in
myo-inositol and ononitol. That both compounds were present
in the extracellular space indicated that myo-inositol might
play a direct role in the facilitation of sodium uptake.
Growth of immature ice plants is severely inhibited by NaCl at
concentrations much lower than those stimulating growth in mature
plants (Adams et al., 1998 Myo-Inositol Unloading, Extracellular Movement, and Myo-Inositol Uptake Myo-inositol is mobile in the extracellular space, likely in all organisms (Garcia-Perez and Burg, 1991), but its movement seems regulated. In yeast, for example, membrane transport of ions is
stimulated during the exponential phase and repressed in the
stationary-phase cultures by the presence of myo-inositol. This regulation is independent of the amount of INPS (INO1 in yeast),
which is not growth-phase dependent (Robinson et al., 1996). In animals
uptake and efflux of osmolytes, including myo-inositol, occurs according to interstitial tonicity (Schmolke et al., 1996a, 1996b). The characteristics of inositol flux into and out of C6 cells,
for example, are similar to those described for volume-regulatory sorbitol and taurine efflux in a number of cell types (Strange et al.,
1993). In plants no myo-inositol efflux or unloading from cells has yet been reported.
Distinguishing Halophytes from Glycophytes One aspect of the results is important in considering the mechanisms of sodium uptake in land plants. From physiological experiments, the only documented sodium-specific transport process is the Na+/H+ antiport system that confines sodium to vacuoles (Barkla and Pantoja, 1996; Tanner and
Caspari, 1996). The components of the transport pathway from the root
to mesophyll vacuoles are not known. Apoplastic entry through the root
tip or a loading step at the boundary at the pericycle/endodermis
followed by passive transport in the transpiration stream and apoplast
has been assumed. However, gradients of ions in the phloem and xylem
have been measured in NaCl-treated barley (Wolf et al., 1990). Their
model implies sodium redistribution within the leaf during the life
cycle, seemingly an adaptive response necessary in the absence of ion
storage cells (e.g. epidermal bladder cells, such as those found in ice
plants; Adams et al., 1998). Under salt stress, potassium is
translocated back to the root when in excess of the plant's
requirement (Jeschke and Pate, 1991). Desbiez et al. (1991) reported
synergy between cation (K+ or
Ca2+) accumulation and myo-inositol
for breaking of the symmetry of bud growth.
2 Present address: Monsanto Life Sciences Co., St. Louis, MO. 63198. * Corresponding author; e-mail bohnerth{at}u.arizona.edu; fax 1-520-621-1697. Received May 14, 1998;
accepted September 8, 1998.
Abbreviations: ITR, myo-inositol transporter. SMIT, sodium/myo-inositol symporter.
We wish to thank Ms. Wendy Chmara for expert HPLC analysis of ions and carbohydrates and Ms. Pat Adams for comments on the manuscript. M.K. gratefully acknowledges receipt of a National Science Foundation-REU fellowship.
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