The Calcium Conundrum. Both Versatile Nutrient and Specific Signal

Abstract

Versatility and specificity are usually mutually exclusive terms. However, as we discuss calcium's role in plant nutrition, we are obliged to contrast the plethora of general housekeeping functions of this element against the ability of calcium (Ca2+) to impart signaling specificity during biological responses (Marschner, 1995). Plants have evolved to rely on the unique properties of Ca2+ for a range of structural, enzymatic, and signaling functions. In this brief update, I will attempt to touch upon the various roles of Ca2+ in plant nutrition, growth, and development. Ca2+ is a relatively large divalent cation, and in contrast to other macronutrients, a high proportion of total Ca2+ is found in the cell walls (apoplast). Some of this Ca2+ is associated to the cell wall, while another portion is exchangeable at the plasma membrane. Additionally, Ca2+ can be found at high concentrations within the vacuole of plant cells. In some tissues of particular plants, Ca2+ can be more than 10% of the dry weight and cause no deleterious effects to plant growth (Marschner, 1995). Juxtaposed against these concentrations of total calcium, the cytosolic-free Ca2+ activity within these cells remains around the 0.1 to 0.2 μ m level. In this update, the first portion will detail the general role of Ca2+ in plant growth and development. In the middle section, we will focus on how almost imperceptible fluctuations in Ca2+ within the cytosol may be translated into plant growth and adaptation. This then leads to the final part of this broad review, to a discussion regarding how biologists are attempting to manipulate Ca2+ levels to improve plant productivity and human nutrition. While we need Ca2+ to build strong bones, plants need Ca2+ to strengthen cell walls and provide stress protection. When human diets are low in Ca2+, this leads to fragile bones or osteoporosis. With plants, soils or media deficient in Ca2+ can cause the disintegration of cell walls and the collapse of the affected tissues (Kirby and Pilbeam, 1984). Ca2+ deficiencies have been associated with bacterial diseases, fruit rotting, and other postharvest problems (Marschner, 1995). Thus, Ca2+ is cited for its beneficial effect on plant vigor and stiffness and also on grain and seed formation (Bennett, 1993). Increasing the Ca2+ content of fruits, for example, by spraying several times with Ca2+ salts during fruit development or by postharvest dipping in CaCl2 solution, leads to an increase in firmness of the fruit and can delay fruit ripening (Bramlage, 1994; Bramlage and Weis, 1994). Ca2+ stabilizes cell membranes by connecting various proteins and lipids at membrane surfaces. Additionally, Ca2+ can be exchanged with other cations (K+, Na+, or H+) during stress responses. To protect the plasma membrane from various stresses, Ca2+ must always be present in the external solution, where it can regulate the selectivity of ion uptake. In fact, when plants are challenged with salinity stress, an increase in the concentration of Ca2+ often can ameliorate the inhibitory effect on growth (Epstein, 1972). In general, Ca2+ is involved in a plethora of plant functions (Marschner, 1995). Ca2+ is involved in cell elongation and cell division, influences the pH of cells, and also acts as a regulatory ion in the source-sink translocation of carbohydrates through its effect on cells and cell walls. A, Blossom-end rot of tomato is caused in part by calcium deficiencies. Scanning electron micrographs of calcium oxalate crystals from Trifolium pratense (B), Vigna unguiculata (C), and Vicia faba (D). Note the different shapes among the various plants. Scale bar = 1 μm (from Nakata, 2003, with permission). The distribution of Ca2+ at the cell wall and plasma membrane is mainly the result of a plethora of binding sites for Ca2+ in the cell walls as well as the carefully regulated transport of Ca2+ into the cytoplasm (Han et al., 2003; see below). Pectins and pectates bind a large portion of Ca2+. As Ca2+ supplies increase within certain cells, the proportion of Ca2+ oxalate increases. In certain situations, oxalate-bound Ca2+ may represent the dominant binding form of Ca2+ (Fig. 1; Nakata, 2003). Intracellular Ca2+ is also found in the endoplasmic reticulum (ER) and chloroplast, and most of the water-soluble calcium is in the vacuole. By virtue of their size and capacity for calcium accumulation, the vacuole is the most prominent sink for calcium storage. Much of our knowledge regarding the role of Ca2+ in cell wall stability and expansion has been obtained from classic physiology experiments. Since it is difficult (impossible?) to generate plant Ca2+ auxotrophs, the onus is now on plant biologists to generate a set of molecular tools to unravel the mechanisms behind these actions (Braam, 1999). Numerous cytosolic proteins bind Ca2+ to dampen free cytosolic Ca2+ concentrations (Sanders et al., 1999; Luan et al., 2002; Sanders et al., 2002). Some of the most prominent Ca2+-binding pr