Focus issue: calcium signaling.

It has beenmy pleasure to act as Guest Editor for this Focus Issue about calcium signaling. Ca is the fifth most abundant element in the Earth’s crust, yet high concentrations are cytotoxic because of precipitation of phosphates, proteins, and DNA. Homeostatic mechanisms to maintain low cellular Ca evolved early, with the ability to pump Ca ions out of the cytosol into the extracellular space being a common feature of cells (Case et al., 2007). Maintaining the 10,000-fold gradient of Ca across the plasma membrane, the largest ionic gradient found in living cells, is energetically expensive; therefore, it was advantageous for cells to coopt the Ca homeostatic machinery for signaling. Changes in the concentration of Ca in the cytosol ([Ca]cyt) and other intracellular spaces participate in complex and dynamic signaling systems in all the kingdoms of life (Case et al., 2007). The Ca signaling toolkit of ion channels, pumps, and regulatory mechanisms was present in the common ancestor of the plants and animals because many of the components are shared between modern animals and the chlorophyte algae. However, at some point in the transition from chlorophyte algae to land plants, selective pressure resulted in the loss of some components of the consensus toolkit, such as entire classes of Ca channel and radiation of alternative mechanisms for Ca signaling in the land plants (Wheeler and Brownlee, 2008). This Focus Issue concentrates on recent advances in the study of Ca signaling in higher plants. The articles describe unique aspects of Ca signaling associated with plantspecific functions in the cell and generated by plantspecific gene families. It is appropriate that a Focus Issue in Plant Physiology emphasizes the unique insights that arise from a community of researchers intent on unraveling the complexity of these dynamic signaling pathways in the most abundant kingdom. My lifetime addiction to the calcium ionwas cemented in a darkroom in the laboratory of Alistair Hetherington, then at Lancaster University, UK, watching in real time the first recording of a stimulus-induced [Ca]cyt oscillation in a guard cell (McAinsh et al., 1995). In this issue, my laboratory reports that oscillating [Ca]cyt signals are not restricted to guard cells, and the pattern of oscillation depends on both the cell and stimulus type, suggesting mechanisms for encoding specificity in signaling networks (Martı́ et al., 2013). Oscillatory changes in nuclear [Ca], induced by nodulation factors, were first described in 1996 by Ehrhardt et al. (1996). The ability of the nucleoplasm to support [Ca] oscillations independently of the cytosol has been considered controversial by some. In this issue, Charpentier and Oldroyd (2013) summarize the compelling evidence that the nucleoplasm can act as an independent compartment for Ca signaling and discuss the potential for decoding nucleoplasm Casignals. The mechanisms for decoding cytosolic Ca signals are described in comprehensive Updates focusing on the calmodulins (Poovaiah et al., 2013), the plant-specific calmodulin-like proteins (Bender and Snedden, 2013), and calcium-dependent protein kinases (Schulz et al., 2013). Ca has been proposed to function in many of the major plant signaling pathways associated with biotic and abiotic stimuli (Dodd et al., 2010). It is very exciting that in this Focus Issue, there are reports of new roles for [Ca]cyt signals in pathways associated with brassinosteroids (Zhao et al., 2013), yeast elicitors (Ye et al., 2013), and gravistimulation (Toyota et al., 2013). The last of these studies includes the astounding achievement of measuring intracellular ion concentrations in an aircraft performing parabolic flight. The signaling pathways that bring about increases in [Ca]cyt are the focus of Updates concerning the interrelationship of nitric oxide (Jeandroz et al., 2013) and reactive oxygen species (ROS), including a new model for long-distance signaling driven by ROS (Steinhorst and Kudla, 2013). New experimental data are presented that demonstrate that ROS activate Ca channels to regulate other ion channels in the plasma membrane during abscisic acid (ABA)-induced stomatal movements (Wang et al., 2013a). A clever use of Ba both as a blocker of K channel activity and as a carrier for charge-through Ca channels, along with the presence of acetate to block Cl conductance, allowedWang et al. (2013a) to measure ABA-induced Ca channel activation at the plasma membrane in intact guard cells with microelectrodes. These data directly link plasma membrane Ca channel activation to the PYR/PYL/RCAR ABA receptors. However, the pyr1 pyl1 pyl2 pyl4 quadruple ABA receptor mutants are not completely insensitive to ABA because in the quadruple mutants, ABA is able to inhibit stomatal opening (Yin et al., 2013). A consequence of the divergence of land plants from the chlorophyte algae is that the channels carrying Ca acrossmembranes can be different in plants and animals. The lack of a molecular identity for themajor Ca influx pathways has been an impediment to progress in plant signaling. New evidence identifying strong candidates for some of the influx pathways associated with Ca signaling in plants, including the annexins, glutamatelike receptors, and cyclic nucleotide-gated channels (CNGCs), is summarized in an Update by Swarbreck et al. (2013). This Focus Issue also contains new evidence for roles for CNGC5 and CNGC6 in guard cells (Wang et al., 2013b) and CNGC2 and CNGC4 in pathogen defense and floral transition (Chin et al., 2013). Many of the manuscripts presenting new data in this Focus Issuemake use of the guard cell as an experimental system. Guard cells are an attractive tool for Ca www.plantphysiol.org/cgi/doi/10.1104/pp.113.900472