Research CommentariesPlant Biology

How Calcium Enhances Plant Salt Tolerance

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Science  19 Jun 1998:
Vol. 280, Issue 5371, pp. 1906-1907
DOI: 10.1126/science.280.5371.1906

Like cells in general, most plant cells accumulate the ion potassium and exclude sodium. The resulting high potassium/sodium ratios in the cells enable potassium to perform essential functions that sodium cannot fulfill. This selectivity in favor of potassium is especially important in the arid and semi-arid regions of the world, where excess sodium salts in the soil cause widespread and often severe problems for crop production. The sodium may compete with potassium in membrane transport and in functions such as enzyme activation, impairing the ability of the plant to grow. For decades, it has been known that another ion, calcium, is required to maintain or enhance the selective absorption of potassium by plants at high concentrations of sodium (1). The mechanisms underlying this crucial action of calcium in protecting plants against the disruptive effects of high sodium concentration have so far eluded us. Now on page 1943 of this issue, a significant advance in our understanding has been made by Liu and colleagues (2), who have identified the molecule that likely mediates this calcium protection.

During membrane transport of ions in any plant exposed to saline conditions, potassium/sodium discrimination is critical at several steps (see the figure). Absorption of potassium initially occurs by an epidermal or cortical cell of the root as it is transported across the outer cell membrane or plasmalemma. After this radial transport across the root, the ion is then delivered into the conducting system of the xylem, in which the element is moved toward and into the shoot. The xylem vessels are apoplastic [that is, composed of extracellular (cell wall) matrix and space], so delivery into this system requires an efflux step, from root cell cytoplasm or “symplast” into the vessels. Movement of potassium and other nutrients takes place in the “transpiration stream,” the movement of water that is ultimately driven by the evaporation or “transpiration” of water, mainly from leaves. Upon arrival in the apoplastic space of the leaf, if it is to function in cellular metabolism, potassium must once again be transported, this time across the plasmalemma of a leaf cell into its cytoplasm. At this point there may be, in addition, redistribution of potassium, most commonly from older to younger, actively growing leaves. This redistribution takes place via the phloem, a cytoplasmic pathway.

Ion flow from soil to leaf.

After initial diffusion into the root cell (apoplastic) wall space (A), the ion is transported across the outer cell membrane or plasma membrane into the cytoplasm of an epidermal or cortical cell (B). (Several layers of cortical cells are represented by only one.) Once in the cytoplasm the ion moves through intercellular connections or plasmodesmata (C) into a cell of the stele and then leaves the “symplast” across the plasma membrane of a stelar cell (D) and enters a vessel, which is, when mature, extracellular or apoplastic space. (Diffusion through cell wall space back into the medium is prevented by the impermeable “Casparian strip.”) The ion then moves into the shoot (E) and eventually is transported across the plasma membrane of, this time, a leaf cell (F) into its cytoplasm.

Nor is that all. At three other potassium transport steps, the plant must differentiate between sodium and potassium. First, inside the cell, potassium is partitioned between the cytoplasm and the vacuole, across the intervening membrane, the tonoplast. While the cytoplasmic potassium concentration is under rather tight homeostatic control, that of the vacuole is more variable. Second, potassium is a major osmoticum of plant cells, an especially crucial feature for plants under high-salt conditions, and one requiring controlled partitioning of the element among organs, tissues, and cell compartments. And third, potassium plays a central role in the opening and closing of stomata, the pores that regulate gas exchange between leaves and the atmosphere. The ion is shuttled into and out of the guard cells, thereby controlling the osmotic movement of water into and out of these cells and, hence, the size of the stomatal aperture and the transpiration rate.

These potassium transport steps are multifarious and complex, and it is likely that all are sensitive to calcium concentrations in the cell. However, because the internal calcium status cannot be manipulated and monitored, most experiments investigating the role of calcium in potassium/sodium transport have had to test the absorption of potassium at various concentrations of potassium, sodium, and calcium in the medium in which the plant roots are bathed. Transport of the ions to the shoot, most often the extent of sodium exclusion from it, is often included.

Experimentation with these methods had reached, or at least approached, a point of diminishing returns in unraveling potassium/sodium transport and salt toleration (and eventually improving plant salt tolerance). Enter the techniques of molecular biology. As a result of the application of molecular biology to this field, several genes and gene products for potassium transport have now been identified and characterized (3). Some operate as high-affinity (mechanism 1) transporters or carriers, whereas others function as low-affinity (mechanism 2) channels (4). How are these regulated by calcium? It is unlikely, given the multiplicity of the sites of potassium/sodium discrimination mentioned earlier, that calcium plays only one role in potassium transport and potassium/sodium selectivity. Rather, responses to salt stress are mediated by signaling pathways in which calcium acts as a second messenger. It is here that the new work contributes.

Now, Liu et al. provide a molecular basis for the calcium sensitivity of potassium/sodium discrimination. In Arabidopsis plants carrying a mutation in the SOS3 gene, the ratio at which potassium and sodium are accumulated is changed to lower potassium/sodium values than in wild-type plants, and the operation of the high-affinity potassium transporter is suppressed. Both abnormal functions are mitigated or abolished by high external calcium concentrations, suggesting that in the mutants there is an impairment in the signaling pathway essential for the normal function of calcium in mitigating salt stress. The deduced amino acid sequence of the SOS3 gene product shows its close affinity to calcium-binding proteins, specifically calcineurin and neuronal calcium sensors of animals (NCS), which can stimulate protein phosphatases or inhibit protein kinases. These versatile proteins participate in some ion transport phenomena in other organisms, lending force to the authors' conclusion that the gene SOS3 mediates the interaction of potassium, sodium, and calcium.

The authors have provided a molecular view of the earlier physiological findings that pinpointed the essential part that calcium plays in potassium/sodium discrimination in plants. The potential of this discovery to advance the pressingly important enterprise of developing salt-tolerant crops is considerable, notwithstanding the fact that Arabidopsis is not itself a salt-tolerant plant. Next, we will need to address the problem of which sites, among the many where potassium/sodium selectivity comes into play, are affected by this gene.

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